Download Acta Medica Okayama

Acta Medica Okayama
Volume 23, Issue 6
1969
Article 6
D ECEMBER 1969
An experimental study on the efferent
connections of the amygdaloid complex in the
cat
Isao Ishikawa∗
Syosuke Kawamura†
Osamu Tanaka‡
∗
Okayama University,
Tokushima University,
‡
Tokushima University,
†
c
Copyright 1999
OKAYAMA UNIVERSITY MEDICAL SCHOOL. All rights reserved.
An experimental study on the efferent
connections of the amygdaloid complex in the
cat∗
Isao Ishikawa, Syosuke Kawamura, and Osamu Tanaka
Abstract
The amygdalofugal fibers were studied III the cat with the silver method of NAUTA-GYGAX.
1. The amygdalofugal fibers are distributed by way of the stria terminalis, the longitudinal association bundle, the inferior thalamic peduncle, and the medial forebrain bundle. 2. The amygdalofugal fibers running through the longitudinal association bundle arise in the lateral principal,
intermediate principal nuclei and the lateral and possibly intermediate parts of the periamygdaloid
cortex, and terminate in the lateral preoptic nucleus, the bed nucleus of the anterior commissure,
the olfactory tubercle, the nucleus of the diagonal band of Broca, the nucleus accumbens, the medial and posterior septal nuclei and the basal part of the head of the caudate nucleus. In addition,
there are scattered fibers coursing along the longitudinal association bundle proper. These fibers
may have a widespread origin from the amygdaloid complex. The longitudinal association bundle
contributes no fibers to the medial forebrain bundle. 3. The fibers, originating from the lateral
principal, intermediate principal and medial principal nuclei, join the medial forebrain bundle to
distribute widely in the lateral hypothalamic nucleus. A few fibers are seen to reach the ventromedial hypothalamic nucleus, and are considered to arise in the medial principal nucleus. 4. By way
of the inferior thalamic peduncle some fibers from the amygdaloid complex course dorsally into
the medial part of the dorsomedial thalamic nucleus at its caudal levels. They may arise widely
from the amygdaloid complex. A few of them extend farther dorsally to reach the lateral habenular
nucleus and the parataenial nucleus. They probably originate from the lateral principal nucleus.
5. The fibers forming the stria terminalis originate from the medial principal nucleus, the medial
nucleus, the periamygdaloid cortex and the cortical nucleus, and are distributed in the bed nucleus
of the stria terminalis and the lateral preoptic nucleus (preoptic component), as well as the medial
preoptic nucleus, the anterior hypothalamic nucleus and the ventromedial hypothalamic nucleus
(supracommissural component). The cortical nucleus, particularly its caudal part, and possibly
the medial part of the periamygdaloid cortex are regarded as the main sources of the stria terminalis fibers ending in the hypothalamic region. The intermediate principal and lateral principal
nuclei do not appear to contribute fibers to the stria terminalis. 6. The ventromedial hypothalamic nucleus receives amygdalofugal fibers both from the medial principal nucleus by way of the
medial forebrain bundle, and from the cortical nucleus via the stria terminalis. 7. In addition to
intrinsic internuclear fibers within the amygdaloid complex, some of the fibers from the complex
∗
c
PMID: 4246441 [PubMed - indexed for MEDLINE] Copyright OKAYAMA
UNIVERSITY
MEDICAL SCHOOL
are distributed to the ventralmost part of the putamen, the medial part of the claustrum, the periamygdaloid cortex, the prepiriform area and the anterior amygdaloid area, but do not reach the
hippocampus.
Ishikawa et al.: An experimental study on the efferent connections of the
Acta Merl. Okayama 23, 519-539 (1969)
AN EXPERIMENTAL STUDY ON THE EFFERENT CONNECTIONS OF THE AMYGDALOID COMPLEX IN THE CAT
Isao ISHIKAWA, Syosuke KAWAMURA and
Osamu TANAKA
Department of Anatomy, Okayama University Medical School, Okayama, Japan
(Director: Prof. K. Niimi) and Department of Internal Medicine, Tokushima
University Medical School, Tokushima, Japan (Director: Prof. T. Aburaya)
Received for publication, August 3, 1969
It has long been known that the efferent fibers from the amygdaloid
complex are distributed largely by way of the stria terminalis. JOHNSTON
(15) first suggested the existence of the amygdalofugal pathway through
the longitudinal association bundle. This was confirmed and extended by
later experimental studies (Fox (9), ADEY and MEYER (l), ADEY et al. (3),
BAN and OMUKAI (4)). These studies revealed that the ventral amygdalofugal pathway is distributed to many basal telencephalic structures, viz.
the preoptic region, the hypothalamus, the thalamus, and the bed nucleus
of the stria terminalis. It is of interest to note that Fox (l0) found in the
monkey amygdalofugal fibers entering the dorsomedial nucleus of the
thalamus by way of the inferior thalamic peduncle. In recent years the
Nauta silver method was found to be the best suited for tracing fiber connections, particularly of unmyelinated and finely myelinated fibers, such
as the amygdalofugal fibers. Recent studies using the Nauta method have
elucidated more precisely the origin, course and termination of amygdalofugal pathways (NAUTA (22), VALVERDE (28,29), POWELL et al. (25), HALL
(14)). However, there is a diversity of opinion among them as to details of
efferent connections of the amygdaloid complex.
The present study was undertaken in an attempt to clarify the exact
distribution of amygdalofugal fibers in the cat by means of the NAUTAGYGAX technique (24) following lesions in the amygdaloid complex. Special
emphasis was placed upon the topical relation of efferent fibers from
different nuclei of the amygdaloid complex.
MATERIAL AND METHODS
Operations were performed on 23 adult cats and five of these, which showed
lesions fairly well localized in the amygdaloid complex, were used in the present
investigation. Unilateral electrolytic lesions were placed in various parts of the
519
Produced by The Berkeley Electronic Press, 1969
1
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
520
I.
ISHIKAWA,
S.
KAWAMURA
& C. TANAKA
amygdaloid complex by the temporal approach under deep Nembutal anesthesia.
After a survival period of 7 to 8 days, the animals were anesthetized and
perfused via the carotid artery with normal saline followed by a solution of 10 %
neutral formalin. The brains were then removed from the skull and sectioned 10
mm thick transversely. These cut blocks were stored in 10 % neutral formalin for
two months, sectioned serially at 35 f.1. on the freezing microtome, and impregnated by the NAuTA-GYGAX (24) silver method.
The classification and terminology of the amygdaloid complex here employed
are based on the investigations of the KOIKEGAMI school, particularly of KARIBE
(16) in carnivores. The site and extent of the lesions in five cases are shown in
Fig. 1.
RESULTS
Cat 38
In this cat the lesion extends throughout the anteroposterior extent of
the left amygdaloid complex, involving the major parts of the medial
principal and intermediate principal nuclei, the medial, intermediate and
lateral parts of the periamygdaloid cortex and parts of the lateral principal
and cortical nuclei.
Fibers from the amygdaloid complex are classified into the ventral
amygdalofugal pathway and the stria terminalis. The former is distributed
through the longitudinal association bundle, the medial forebrain bundle
and the inferior thalamic peduncle. The degenerated fibers forming the
ventral pathways run dorsomedially to pass through the sublenticular gray,
in which a few fibers appear to terminate. A group of fine, densely
crowded, degenerated fibers course rostrally through the longitudinal
association bundle, with some medium-sized and rather fine scattered fibers
along them. It proceeds farther rostrally just ventral and ventromedial to
the internal capsule to reach the lateral preoptic nucleus. Passing through
this nucleus, it begins to disperse medially and dorsomedially in the whole
area of the lateral preoptic nucleus. At anterior levels of the anterior
commissurs the degenerated fibers in the dorsomedial part of the lateral
preoptic nucleus continue dorsomedially, and most of them are found to
terminate in the bed nucleus of the anterior commissure. Very few fibers
enter the ventral part of the anterior commissure to course medially, but
their final destination cannot be followed. Rostrallya considerable num·
ber of degenerated fibers coursing through the lateral part of the lateral
preoptic nucleus are distributed diffusely in the olfactory tubercle and the
anterior amygdaloid area. A few of them can be traced to the subcortical
region of the anterior sylvian gyrus. In addition, some degenerated fibers
in the ventromedial part of the lateral preoptic nucleus, passing rostrally,
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
2
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
521
run medially and dorsomedially through the diagonal band of Broca,
where a few fibers are found to terminate, and enter the ventral part of
the medial septal nucleus at anterior levels of the head of the caudate
nucleus.
At anterior levels of the optic chiasma, the degenerated fibers coursing medially through the sublenticular gray join the medial forebrain
bundle and run caudally in rather compact bundles to enter the lateral
hypothalamic nucleus. Proceeding caudally, the degenerated fibers are
distributed widely to this nucleus, but gradually they are confined to its
ventral part. As the ventromedial hypothalamic nucleus appears, a few of
them proceed ventromedially to enter its anterolateral part. Most of the
degenerated fibers continue further caudally through the lateral hypothalamic nucleus, gradually decreasing in number. They disappear at
the level of the anterior pole of the mammillary body.
At levels of the rostral third of the optic chiasma, scattered degenerated fibers passing dorsally from the sublenticular region enter the inferior
thalamic peduncle. The majority of them course dorsocaudally through
this fiber bundle to distribute in the posterior region of the dorsomedial
thalamic nucleus, with a few fibers proceeding further dorsally to the
ventral part of the lateral habenular nucleus. Within the dorsomedial
nucleus the degeneration is confined to its medial (magnocellular) part.
During their course through the inferior thalamic peduncle some of the
degenerated fibers leave it to pass through the anteromedial nucleus and
reach the ventral part of the parataenial nucleus. A few fibers appear to
end in the paracentral nucleus at posterior levels of the optic chiasma.
The fibers entering the stria terminalis arise from the posterior part
of the lesion and run caudally ventrolateral and lateral to the optic tract.
They then curve dorsally along the tail of the caudate nucleus to lie dorsc>lateral to the thalamus. The degenerated fibers in the stria terminalis
can be differentiated into a dorsomedial and a ventrolateral division.
The former consists of fine, densely arranged fibers, while the latter is
composed of medium-sized, rather scattered fibers. These two divisions
together pass rostrally to reach the anterior commissural levels without
giving off any fibers and divide into the preoptic (lateral) and supracommissural (medial) components. The preoptic component, derived from the
ventrolateral division, courses ventrally to end largely in the bed nucleus
of the stria terminalis dorsolateral to the posterior border of the anterior
commissure, but some fibers proceed further ventralward lateral to the
anterior commissure to end in the medial part of the lateral preoptic
nucleus. The supracommissural component, a direct continuation of the
Produced by The Berkeley Electronic Press, 1969
3
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
522
I. ISHIKAWA, S.
KAWAMURA
& O. TANAKA
Cat 48
Cat 38
Cat 61
Cat 60
Cat 40
Fig. I Drawings of transverse sections showing the site and extent of lesions in the
amygdaloid complex in each case. The lesion is indicated in solid black.
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
4
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
523
dorsomedial division, swings ventrocaudally in front of the anterior
commissure to enter the medial preopic nucleus, where some fibers terminate. Most of the degenerated fibers of the supracommissural 'component
pass through this nucleus to reach the anterior hypothalamic nucleus, in
which many fibers are found to terminate. However, some of them proceed
further caudally to distribute in the ventromedial part of the lateral hypothalamic nucleus. During their courseva few fibers turn ventrally to enter
the ventromedial hypothalamic nucleus, where these fibers are intermingled with the fibers coming by way of the medial forebrain bundle.
Medium to coarser degenerated fibers arising in the lateral part of the
lesion are found to join the external capsule and proceed dorsally to enter
the posterior limb of the anterior commissure. Passing rostrally, they turn
medially and cross in the dorsal portion of the anterior commissure. They
can be traced as far as the sublenticular region of the opposite side, but
their farther course cannot be traced. A few degenerated fibers are
Abbreviations
Aa, Anterior amygdaloid area
Ac, Nucleus accumbens
Bca, Bed nucleus of anterior commissure
Bst, Bed nucleus of stria terminalis
C, Central nucleus
Ca, Anterior commissure
Cd, Head of caudate nucleus
Ch, Optic chiasma
Ci, Internal capsule
CI, Clautsrum
Co, Cortical nucleus
Dg, Nucleus of diagonal band
F, Fornix
Ha, Anterior hypothalamic nucleus
Hbl, Lateral habunular nucleus
HI, Lateral hypothalamic nucleus
Hvm, Ventromedial hypothalamic
nucleus
Ip, Intermediate principal nucleus
ITP, Inferior thalamic peduncle
LAB, Longitudinal association
Produced by The Berkeley Electronic Press, 1969
bundle
Lp, Lateral principal nucleus
M, Medial nucleus
Md, Dorsomedial thalamic nucleus
MFB, Medial forebrain bundle
Mp, Medial principal nucleus
Paml! Lateral part of periamygda.
loid cortex
Pam 2, Intermediate part of periamygdaloid cortex
Pam s, Medial part of periamygdaloid cortex
Pir, Piriform cortex
Pol, Lateral preoptic nucleus
Porn, Medial preoptic nucleus
Pt, Parataenial nucleus
Pu, Putamen
Sm, Medial septal nucleus
Sp, Posterior septal nucleus
ST, Stria terminalis
Tol, Olfactory tubercle
Vm, Medial ventral nucleu~
5
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
524
I.
ISHIKAWA,
S.
KAWAMURA
& O. TANAKA
found to enter the chustrum without coursing to the anterior commissure.
Within the claustrum degenerated fibers are scattered in its medial part,
but they cannot be seen at levels rostral to the septum.
A few degenerated fibers from the lesion take a direct dorsal course
to distribute in the ventral and lateral part of the putamen at levels caudal
to the anterior commissure.
Within the amygdaloid complex a large number of degenerated fibers
are found in the lateral principal and central nuclei, which are not in.
volved in the lesion, but scarcely any degeneration is discernible in the
cortical and medial nuclei.
Cat 48
The lesion in this cat is situated for the most part in the intermediate
principal nucleus of the left amygdaloid complex and involves the medial
part of the periamygdaloid cortex and parts of the medial principal and
cortical nuclei.
As compared with cat 38, the degenerated fibers in the longitudinal
association bundle proper are relatively few in number, while those around
the bundle are abundant. Passing rostrally, the degenerated fibers as a
whole spread medially to reach the medial part of the lateral preoptic
nucleus, where some fibers are found to terminate. Most of the degenerated fibers run rostrally through the hteral preoptic nucleus to distribute
widely in the prepiriform area, with some fibers entering the medial part
of the olfactory tubercle. At the middle level of the anterior commissure
the degenerated fibers in the lateral preoptic nucleus course in two direc·
tions: dorsomedial and ventromedial. Some of the dorsomedially running
fibers are directed to the bed nucleus of the anterior commissure, but the
majority pass dorsally to spread dorsomedially to the nucleus accumbens
and dorsolaterally to the ventromedial part of the head of the caudate
nucleus at levels rostral to the anterior commissure. The ventromedially
running fibers course rostrally to join the diagonal band of Broca. Most
of them proceed dorsomedially to enter the ventral part of the medial
septal nucleus at rostral levels of the head of the caudate nucleus, though
some fibers are found to end in the nucleus of the diagonal band.
At levels of the optic chiasma the degenerated fibers joining the
medial forebrain bundle course caudally through the lateral hypothalamic
nucleus, sending some fibers to the lateral part of the anterior hypothalamic nucleus. At rostral levels the degenerated fibers are distributed widely
in the lateral hypothalamic nucleus, but caudally they decrease in number
and are limited to its ventral part. Very few fibers are found to enter the
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
6
Ishikawa et al.: An experimental study on the efferent connections of the
525
Efferent Connections of Cat Amygdala
ventromedial hypothalamic nucleus.
Some degenerated fibers enter the inferior thalamic peduncle to course
caudodorsally and are distributed in the medial part of the dorsomedial
thalamic nucleus at caudal levels of the mamillary body, as in cat 38.
However, there are no fibers passing through the dorsomedial nucleus
to the lateral habenular nucleus.
Cat 38
Ch
Cat 48
Fig. 2 Fiber degeneration observed in cats 38 and 48. Coarse dots indicate degenerating fibers of passage, fine stripple preterminal degeneration.
The degenerated fibers coursing through the stria terminalis arise in
the posterior portion of the lesion, that is, the cortical nucleus and the
medial part of the medial principal nucleus. They are relatively few in
Produced by The Berkeley Electronic Press, 1969
7
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
526
1. ISHIKAWA, S.
KAWAMVRA
& O. TANAKA
number as compared with cat 38. The degenerated fibers run through the
stria terminalis turning caudodorsally and then rostrally in association with
the tail of the caudate nucleus to reach the level of the caudal border of
the anterior commissure. At this level the degenerated fibers divide into
the supracommissural and preoptic components. The preoptic component
takes a ventral course just lateral to the anterior commissure to end in the
bed nucleus of the anterior commissure and the medial part of the lateral
preoptic nucleus. The supracommissural component, after sending some
fibers to the posterior septal nucleus, runs ventromedially to turn caudally
in front of the anterior commissure. It then passes ventromedial to the
fornix through the medial preoptic nucleus, giving off in course fibers
to this nucleus, and e!1ters the anterior hypothalamic nucleus, where it
disappears at the rostralmost level of the infundibulum. During its course
a small number of degenerated fibers diverse from it to pass ventrolaterally
to the ventromedial hypothalamic nucleus. In addition, very few fibers
are seen running medially into the arcuate nucleus.
A small number of medium-sized fibers are seen running dorsally from
the lesion to pass through the ventral part of the external capsule into the
claustrum. In this case there are no fibers entering the anterior commissure.
As in cat 38, some fine and medium-sized degenerated fibers are
directed dorsally from the lesion to the putamen and are scattered in the
ventral and lateral part of the putamen at levels of the optic chiasma.
Within the amygdaloid complex degenerated preterminals are scattered in the intermediate principal, medial principal and central nuclei,
but not in the cortical and medial nuclei. In the lateral part of the periamygdaloid cortex a few degenerated preterminals are found.
Cat 60
The lesion is placed in the lateral principal nucleus, involving the
dorsalmost part of the intermedi<l:te principal nucleus and part of the
medial nucleus and the lateral part of the periamygdaloid cortex.
The degenerated fibers forming the ventral amygdalofugal pathway
are directed dorsally and dorsomedially. Most of them course through
and along the longitudinal association bundle. In this cat fibers passing
through this bundle are abundant, whereas those coursing along it are
much sparser than those found in cat 48. Proceeding rostrally, the degenerated fibers of the longitudinal assodiation system run medially and
dorsomedially. At the level of the anterior border of the optic chiasma
they divide into two distinct groups: medial and lateral. At about the
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
8
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
527
middle level of the anterior commissure the medial group of fibers extend
shell-like mediolaterally ventral to the internal capsule. Passing rostrally,
the majority of the fibers of this group run ventromedially to join the
diagonal band of Broca and end in the medial septal nucleus at levels of
the head of the caudate nucleus, giving off fibers to the nucleus of the
diagonal band and the medial part of the lateral preoptic nucleus. On
the other hand, a small number of fibers run dorsally from the medial
group and are scattered in the ventral part of the head of the caudate
nucleus and the lateral part of the posterior septal nucleus. At this level a
few fibers are seen running medially through the ventral portion of the
anterior commissure to the contralateral side.
The lateral group of fibers proceed rostrally to distribute largely in
the anterior amygdaloid and prepiriform areas and partly in the lateral
part of the olfactory tubercle.
The degenerated fibers joining the medial forebrain bundle are
relatively few in number as compared with those of cats 38 and 48. Proceeding caudally, they take a medial course and distribute in the lateral
hypothalamic nucleus. They decrease in number caudally and can be
traced as far as the anteriormost level of the mamillary body. In this case,
none appear to enter the ventromedial hypothalamic nucleus.
Cat 60
Fig. 3 Fiber degeneration in cat 60. Symbols as in Fig. 2.
Some degenerated fibers are seen coursing through the inferior thalamic peduncle to the dorsomedial thalamic nucleus as in cat 38, but are
somewhat smaller in amount.
Produced by The Berkeley Electronic Press, 1969
9
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
528
I.
ISHIKAWA,
S.
KAWAMURA
& O.
TANAKA
The degenerated fibers passing by way of the stria terminalis arise
from the caudal part of the lesion, mainly from the medial nucleus. They
are much smaller in amount than those in the previous cases. The degenerated fibers course through the stria terminalis closely associated to the
tail of the caudate nucleus (ventrolateral division). It should be noted that
no degenerated fibers are found in that portion of the stria terminalis
which lies just beneath the ventricle (dorsomedial division). As the head of
the caudate nucleus is reached, most of the degenerated fibers pass ven·
trally through its medial portion to end in the bed nucleus of the stria
terminalis. A few fibers, however, terminate in the medial part of the
lateral preoptic nucleus, where they are intermingled with the fibers
coming by way of the longitudinal association bundle. In this case there
are no fibers passing through the medial preoptic nucleus to the hypothalamic nuclei.
Also in this case many medium-sized degenerated fibers are seen
coursing dorsally from the lateral part of the lesion along the lateral periphery of the amygdaloid complex. Some of them enter the posterior limb
of the anterior commissure to cross to the contralateral side. Other fibers
enter the external capsule to end in the claustrum.
Cat 61
The lesion attains its maximal size at middle levels of the optic chiasma,
covering most of the medial principal nucleus, the medial and intermediate
parts of the periamygdaloid cortex and the ventral small part of the intermediate principal nucleus. Caudally it decreases in size and is confined
to the medial part of the medial principal nucleus, the ventromedial part
of the cortical nucleus and the intermediate part of the periamygdaloid
cortex.
The degenerated fibers forming the ventral amygdalofugal pathway
are directed dorsally and then course rostrally ventral to the entopeduncular nucleus.
In this cat the degenerated fibers running through the longitudinal
association bundle proper are few in number, while those around it are
abundant. The degenerated fibers as a whole course rostrally, forming
a single mass of diffusely scattered fibers. As the anterior commissure
appears, a few of the medially situated fibers sweep dorsolaterally around
the internal capsule to spread into the basal part of the head of the caudate
nucleus. Most of the medial fibers, however, run more rostrally and
terminate in the medial part of the lateral preoptic nucleus and the bed
nucleus of the anterior commissure, with a few fibers joining the diagonal
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
10
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
529
band of Broca to end in the medial septal nucleus. On the other hand,
the laterally situated fibers pass rostrally to distribute in the lateral part of
the lateral preoptic nucleus, the dorsal part of the olfactory tubercle and
the prepiriform area.
The degenerated fibers joining the medial forebrain bundle are distributed in the lateral hypothalamic nucleus. In the anterior part of this
nucleus degenerated fibers are found throughout, but caudally decrease in
number and disappear at the level of the anterior extremity of the mamillary body.
Some degenerated fibers are seen to enter the inferior thalamic
peduncle from the sublenticular region at anterior levels of the optic
chiasma. They run dorsocaudally to distribute in the medial part of the
dorsomedial thalamic nucleus.
From the posterior portion of the lesion, that is, the medial part of
the medial principal nucleus and the ventrolateral part of the cortical
nucleus, a large number of degenerated fibers are found entering the stria
terminalis and reach the anteriormost level of the anterior commissure. At
this level a few fibers terminate in the lateral part of the bed nucleus of
the stria terminalis, but the majority loop around the anterior commissure
and then swing caudally to pass through the medial preoptic nucleus and
enter the anterior hypothalamic nucleus. Within these nuclei a considerable number of fibers terminate, but the remaining fibers run further
caudally through the anterior hypothalamic nucleus medial to the fornix
and terminate in the dorsal part of the anterior half of the ventromedial
hypothalamic nucleus.
Cat 40
In this cat the lesion destroys partly the intermediate and lateral parts
of the left peri3.mygdaloid cortex, At more caudal levels a localized small
lesion is found in the medial principal nucleus.
Fine degenerated fibers, leaving the anterior part of the lesion in
the intermediate part of the periamygdaloid cortex, run dorsomedially
and enter the longitudinal association bundle. The fibers in this bundle
are large in number, but a considerable number of fibers are scattered
diffusely around it. As the anterior commissure appears, the degenerated
fibers of the longitudinal association bundle form a transversely elongated
mass of fibers, which does not divide into two groups, in contrast to cat
60. The medial portion of this mass, although projecting a few fibers to
the basal part of the caudate nucleus, proceeds rostrally to distribute
widely in the lateral preoptic nucleus. Passing more rostrally, it terminates
Produced by The Berkeley Electronic Press, 1969
11
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
530
I.
ISHIKAWA,
S.
KAWAMURA
& O.
TANAKA
in the lateral preoptic nucleus, the bed nucleus of the anterior commissure
and the r!ucleus of the diagonal band, with a few fibers running through
the diagonal band to the medial septal nucleus. From the lateral portion
of the mass, degenerated fibers are directed laterally to distribute in the
olfactory tubercle and the prepiriform area.
Some degenerated fibers join the medial forebrain bundle to run
caudally and distribute widely in the anterior part of the lateral hypothalamic nucleus. Very few of them pass medially and cross through the
commissure of Meynert to the contralateral side, but their farther course
cannot be followed.
The medium-sized degenerated fibers from the lateral part of the
lesion enter the posterior limb of the anterior commissure to cross through
the dorsal portion of the commissure to the contralateral side, although
their ultimate distribution cannot be established.
From the posterior part of the lesion, involving the intermediate part
of the periamygdaloid cortex and the medial principal nucleus, a few
fibers run dorsomedially to enter the stria terminalis and pass around the
thalamus until the anterior commissure level is attained. They then proceed
ventrally to end largely in the bed nucleus of the stria terminalis ar:d partly
in the medial preoptic nucleus, but no fibers can be traced to the hypothalamus.
DISCUSSION
Longitudinal association bundle
In all our cases degenerated fibers are seen running through or along
the longitudinal association bundle. I n cats 40, 60 and 38 they are consistently found in the longitudinal association bundle proper. In cats 60
and 38 the lesions involve the intermediate principal nucleus, the lateral
principal nucleus and the periamygdaloid cortex, particularly its lateral
part. In cat 40, however, the lesion is localized roughly to the lateral and
intermediate parts of the periamygdaloid cortex, and does not involve the
lateral and intermediate principal nuclei. This indicates that the longitudinal association bundle receives fibers from the lateral and possibly from
the intermediate part of the periamygdaloid cortex, in addition to the
intermediate and lateral principal nuclei. The contribution of the intermediate principal nucleus to the longitudinal association bundle is also
evidenced by the fact that degenerated fibers are found in this bundle in
cat 48 where the lesion is almost confined to the intermediate principal
nucleus. On the other hand, only very few fibers are seen in this bundle
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
12
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
531
in cat 61 with the lesion involving almost all of the medial principal
nucleus and the medial and intermediate parts of periamygdaloid cortex.
From this fact it may be said that scarcely any contribution to this bundle
is made by the medial principal nucleus and the medial part of the peri.
amygdaloid cortex. In all our cases scattered degenerated fibers are seen
running forward along the longitudinal association bundle. They may
originate widely from the amygdaloid complex, including the cortex of the
piriform lobe.
It is generally accepted that the amygdaloid complex contributes
fibers to the longitudinal association bundle. Fox (9), studying by means
of the Marchi method in the rat, stated that the longitudinal association
bundle arises in the large-celled basal amygdaloid nucleus (intermediate
principal nucleus). HALL (14) studied the efferent connections of the
amygdala in the cat and stated that the longitudinal association bundle
originates not only in the basal nucleus but also in the lateral nucleus of
the amygdaloid complex. She found that the contribution of the basal
nucleus is considerably greater than that of the lateral, and the fibers
from the lateral nucleus are more thinly myelinated. VALVERDE (29)
agreed with the above·mentioned view that the bundle originates mainly
in the basolateral nucleus. BAN and OMUKAI (4), using the Marchi method
in the rabbit, stated that the longitudinal association bundle arises in the
lateral part of the basal nucleus, the anterior part of the lateral nucleus
and the periamygdaloid cortex. Our results agree roughly with those of
BAN and OMUKAI.
According to our results, degenerated fibers coursing through or along
the longitudinal association bundle are distributed to the anterior amygdaloid and the prepiriform areas, the lateral preoptic nucleus, the bed
nucleus of the anterior commissure, the olfactory tubercle, the nucleus of
the diagonal band of Broca, the nucleus accumbens and the medial and
posterior septal nuclei. In addition, some degenerated fibers are seen to
reach the basal part of the head of the caudate nucleus in cats 48, 60 and
61.
Fox (9) and HALL (14) stated that the longitudinal association bundle
arising from the basal nucleus shDws a partial division into lateral, and
medial components. According to HALL, the lateral component terminates
in the lateral two-thirds of the preoptic region, th~ bed nucleus of the
anterior commissure and the substantia innominata, while the medial
component ends in the medial two-thirds of the preoptic region and the
bed nucleus of the anterior commissure. In most of our cases where the
longitudinal association bundle is severely degenerated (cats 40 and 38),
Produced by The Berkeley Electronic Press, 1969
13
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
532
I.
IsHIKAWA,
S. KAWAMURA & O. TANAKA
c;-----
Fig. 4 Diagram showing the distribution of amygdalofugal fibers
in the cat. Fibers from the lateral nuclear group of the amygdaloid
complex are shown by solid lines; those from the medial nuclear group
by dotted lines.
the longitudinal association bundle shows scarcely any divivion. In cat 60,
however, it divides clearly into two components. The medial component
terminates in the ventromedial part of the head of the caudate nucleus,
the lateral part of the posterior septal nucleus, the lateral preoptic area,
the nucleus of the diagonal band of Broca and the medial septal nucleus,
while the lateral component ends in the anterior amygdaloid area, the
prepiriform area and the lateral part of the olfactory tubercle.
On the basis of observations made on normal preparations, JOHNSTON
(15) and Fox (8) stated that the longitudinal association bundle contributes
fibers to the medial forebrain bundle. Later papers, including the experimental study of Fox (9), denied such a contribution. Our results are also
negative.
Medial forebrain bundle
In all our cases with lesions of the amygdaloid complex, the degene-
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
14
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
533
rated fibers coursing through the medial forebrain bundle are distributed
to the hypothalamus. They are widely distributed to the lateral hypothalamic nucleus. Proceeding caudally, they gradually decrease in number
to disappear at levels of the mamillary body. The lateral principal, intermediate principal and medial principal nuclei are regarded as the probable
sources of the amygdalofugal fibers to the medial forebrain bundle. In
addition, a few fibers are seen running medially to reach the ventromedial
hypothalamic nucleus in cats 38, 48, 61 and 40, where the medial principal
nucleus is involved in the lesion. In cat 40 the lesion involves only the
medial principal nucleus and the periamygdaloid cortex. These facts indicate that the ventromedial hypothalamic nucleus receives fibers largely,
if not exclusively, from the medial principal nucleus.
HALL (14) stated that the diffuse fibers from the lateral nucleus course
directly medially inferior to the ansa lenticularis to join the medial forebrain bundle and are distributed throughout the lateral hypothalamus.
VALVERDE (29) designated such a group of fibers the medial amygdalohypothalamic pathway and considered it to originate largely from the area
amygdaloidea anterior and the medial part of the central nucleus. NAUTA
(22) described the ventral amygdalofugal fibers coursing to the lateral
preoptic and hypothalamic regions. These fibers terminate diffusely among
cell groups scattered between the longitudinal fibers of the medial forebrain bundle. Only a few of them accompany the bundle caudalward to
distribute in the lateral hypothalamus at infundibular levels or farther
caudally. Fox (9), BAN and OMUKAI (4), and ADEY and MEYER (1) did
not describe the amygdalofugal fibers joining the medial forebrain bundle.
Inferior thalamic peduncle
Some fibers from the amygdaloid complex course dorsally into the
dorsomedial thalamic nucleus by way of the inferior thalamic peduncle.
They are distributed in the medial part of the dorsomedial nucleus at its
caudal levels in all our cases. Some of them are found to extend farther
dorsally to reach the lateral habenular nucleus and the parataenial nucleus
in cats 38 and 60, where the lesions involve more or less the lateral principal nucleus. These data suggest that the amygdalofugal fibers to the
dorsomedial nucleus have a relatively widespread origin from the amygdoloid complex, and that those to the lateral habenular and parataenial
nuclei arise from the lateral principal nucleus.
Based on the Marchi experiments in the monkey, Fox (l0) first
described the amygdalofugal fibers coursing directly to the dorsomedial
nucleus by way of the inferior thalamic peduncle. NAUTA (22) confirmed
Produced by The Berkeley Electronic Press, 1969
15
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
I. ISHIKAWA, S.
534
KAWAMURA
& O. TANAKA
Fox's observations and found these fibers to terminate in the medial,
magnocelluar part of the dorsomedial nucleus. He could not identify the
contributing amygdaloid nuclei with certainty, but considered the basal
and lateral nuclei to be the most likely sources of origin of the amygdalothalamic connections. HALL (14), however, was not able to demonstrate
direct amygdalotha1amic fibers following lesions in the basal and lateral
nuclei in the cat. VALVERDE (28, 29) followed the amygdalothalamic fibers
of the cat to the posteromedial part of the dorsomedial nucleus. According
to him, these fibers may arise in the area amygdaloidea anterior and little,
if any, contribution can be expected from the remaining amygdaloid
nuclei. On the other hand, NAUTA found some sparse termination of
amygdalofugal fibers in the rostral midline region and the paracentral
intralaminar nucleus, in addition to the dorsomedial nucleus. However,
such terminations cannot be observed in our experiments, except for cat
38 where a few fibers appear to terminate in the paracentral nucleus.
Stria terminalis
In cats 38, 48 and 61 the amygdalofugal fibers forming the stria
terminalis are distributed in the bed nucleus of the stria terminalis and
the lateral preoptic nucleus (preoptic component), as well as the medial
preoptic area, the anterior hypothalamic nucleus and the ventromedial
hypothalamic nucleus (supracommissural component). In cats 60 and 40,
where the cortical nucleus and the medial part of the periamygdaloid
cortex are intact, the degenerated fibers are relatively few in the stria
terminalis and end mostly in the bed nucleus of the stria terminalis and
partly in the lateral preoptic nucleus. This indicates that the cortical
nucleus, particularly its caudal part, and possibly the medial part of the
periamygdaloid cortex are the main sources of the stria terminalis fibers
ending in the hypothalamic region (supracommissural component). It is
evident from the above cases that the fibers from the medial principal
nucleus and the medial nucleus enter the stria terminalis, but do not
extend to the hypothalamic region (preoptic component). The intermediate
principal nucleus does not appear to contribute fibers to the stria terminalis.
In cat 48 no degenerated fibers are found to enter the stria from the
anterior portion of the lesion lying largely in the intermediate principal
nucleus. Although a few degenerated fibers are seen in the stria terminalis
in cat 60, they arise from the posterior portion of the lesion involving the
medial principal and cortical nuclei. There is no evidence that the lateral
principal nucleus contributes fibers to the stria terminalis.
There has been no general agreement as to the exact origin and termi-
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
16
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
535
nation of the stria terminalis fibers from the amygdaloid complex. Fox (9)
stated that a large portion of the stria terminalis originates in the basal
amygdaloid nucleus, particularly its caudal end, and projects to the
septum, the preoptic region and the vicinity of the paraventricular nucleus
of the hypothalamus. He failed to trace degeneration in the stria after
lesions in the lateral nucleus of the amygdala. According to observations
of ADEY and MEYER (1) in the monkey, the stria terminalis fibers arise
mainly in the basal amygdaloid nucleus, and degeneration is found prin.
cipally in the hypothalamic and supracommissural components of the stria,
which appear to be more closely related to the posterior basolateral parts
of the amygdaloid complex than to the corticomedial group. HALL (14)
stated that the basal nucleus in the cat contributes fibers to the stria terminalis and projects fibers to the bed nucleus of the stria terminalis and the
anterior commissure. NAUTA (22) described the stria terminalis in the
monkey as originating mostly in the caudal half of the amygdaloid complex. Fibers arising most rostrally in the complex appear to terminate
largely in the bed nucleus of the stria terminalis. Other fibers of more
caudal region form a prominent preoptico-hypothalamic component distri·
buting fibers to the medial preoptic nucleus, the anteior hypothatamic
nucleus and the region of the nucleus supraopticus diffusus. Our results
reveal that the supracommissural component corresponding to NAUTA'S
preoptico-hypothalamic component originates from the cortical nucleus,
particularly its caudal part. BAN and OMUKAI (4) stated that the supracommissural component originates in the medial nucleus, the cortical
nucleus and the small·celled medial part of the basal nucleus, and termi·
nates in the bed nucleus of the stria terminalis and the anterior commissure,
the septal area and the rostral part of the ventromedial hypothalamic
nucleus, while the preoptic component, arising in the large.celled lateral
part of the basal nucleus and the periamygdaloid cortex, terminates in
the lateral preoptic area.
Most of the authors claimed that the stria terminalis fibers are distributed to the ventromedial hypothalamic nucleus (ADEY and MEYER (1),
BAN and OMUKAI (4), HALL (14)), while a few workers denied such a connection (NAUTA (22), VALVERDE (29)). According to our results, the ven·
tromedial hypoth,::l.1amic nucleus receives amygdalofugal fibers by way of
both the medial forebrain bundle and the stria terminalis.
Anterior commissure
Since JOHNSTON'S (15) description in normal bat material, the commissural component of the stria terminalis has been described by a number
Produced by The Berkeley Electronic Press, 1969
17
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
536
I. IsHIKAWA, S.
KAWAMURA
& O.
TANAKA
of authors. NAUTA (22), studying experimentally in the monkey, followed
a few fibers of the stria terrninalis across the midline in the dorsal stratum
of the anterior commissure, but could not determine their termination.
However, no stria terminalis fibers are seen to cross in the anterior commissure in all of our experiments. In studies of normal material YOUNG (30)
found that the posterior limb of the anterior commissure serves to interconnect the amygdaloid nuclei, particularly the lateral, of the two sides.
In cats 40, 60 and 38 of our cases also some fibers are seen running dorsally
from the lesion to join the posterior limb of the anterior commissure and
can be traced to the sublenticular gray of the opposite side. It is, however,
difficult to determine whether or not they arise in the amygdaloid complex.
In agreement with observations of HALL (14) a few fibers of the longitudinal association bundle course dorsomedially to cross in the anterior limb
of the anterior commissure to the contralateral side. They may arise in
the intermediate principal and lateral principal nuclei.
Other amygdaiofugai pathways
NAUTA (22) found degenerated fibers in the claustrum and the lateral
zone of the putamen following lesions in the amygdaloid complex in the
monkey. According to VALVERDE (29), some fine degenerated fibers are
seen to end in the posterior pole of the claustrum in the cat. Coarse fibers
are also observed in the putamen, but they are probably fibers interrupted
by the needle track. In addition, the electro-physiological study of ADEY
et ai. (2) suggested the correlation between the amygdaloid complex and
the globus pallidus. In all our cases some degenerated fibers can be traced
to the ventralmost part of the putamen and the medial part of the claustrum.
KOIKEGANI et ai. (19) stated that the stimulation of the medial principal
nucleus and cortical nucleus (medial nuclear group) gives rise to sympathetic responses, while the stimulation of the lateral nuclear group produces
parasympathetic or no responses. These results are considered to be closely
related to the fiber connections of the amygdaloid complex. It is of interest
to note that the medial nuclear group tends to send fibers by way of the
stria terminalis to the medial hypothalamus (B-sympathetic zone of KUROTSU), while the lateral nuclear group contributes fibers to the medial
forebrain bundle and projects to the lateral hypothalamus (C-parasympathetic zone of KUROTSU).
SUMMARY
The amygdalofugal fibers were studied
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
III
the cat with the silver
18
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
537
method of NAUTA-GYGAX.
1. The amygdalofugal fibers are distributed by way of the stria
terminalis, the longitudinal association bundle, the inferior thalamic
peduncle, and the medial forebrain bundle.
2. The amygdalofugal fibers running through the longitudinal association bundle arise in the lateral principal, intermediate principal nuclei
and the lateral and possibly intermediate parts of the periamygdaloid cortex, and terminate in the lateral preoptic nucleus, the bed nucleus of the
anterior commissure, the olfactory tubercle, the nucleus of the diagonal
band of Broca, the nucleus accumbens, the medial and posterior septal
nuclei and the basal part of the head of the caudate nucleus. In addition,
there are scattered fibers coursing along the longitudinal association bundle
proper. These fibers may have a widespread origin from the amygdaloid
complex. The longitudinal association bundle contributes no fibers to the
medial forebrain bundle.
3. The fibers, originating from the lateral principal, intermediate
principal and medial principal nuclei, join the medial forebrain bundle to
distribute widely in the lateral hypothalamic nucleus. A few fibers are
seen to reach the ventromedial hypothalamic nucleus, and are considered
to arise in the medial principal nucleus.
4. By way of the inferior thalamic peduncle some fibers from the
amygdaloid complex course dorsally into the medial part of the dorsomedial thalamic nucleus at its caudal levels. They may arise widely from
the amygdaloid complex. A few of them extend farther dorsally to reach
the lateral habenular nucleus and the parataenial nucleus. They probably
originate from the lateral principal nucleus.
5. The fibers forming the stria terminalis originate from the medial
principal nucleus, the medial nucleus, the periamygdaloid cortex and the
cortical nucleus, and are distributed in the bed nucleus of the stria terminalis and the lateral preoptic nucleus (preoptic component), as well as the
medial preoptic nucleus, the anterior hypothalamic nucleus and the ventromedial hypothalamic nucleus (supracommissural component). The cortical
nucleus, particularly its caudal part, and possibly the medial part of the
periamygdaloid cortex are regarded as the main sources of the stria terminalis fibers ending in the hypothalamic region. The intermediate principal
and lateral principal nuclei do not appear to contribute fibers to the stria
terminalis.
6. The ventromedial hypothalamic nucleus receives amygdalofugal
fibers both from the medial principal nucleus by way of the medial forebrain bundle, and from the cortical nucleus via the stria terminalis.
Produced by The Berkeley Electronic Press, 1969
19
Acta Medica Okayama, Vol. 23 [1969], Iss. 6, Art. 6
538
I. IsHIKAWA, S. KAWAMURA & O. TANAKA
7. In addition to intrinsic internuclear fibers within the amygdaloid
complex, some of the fibers from the complex are distributed to the
ventralmost part of the putamen, the medial part of the claustrum, the
periamygdaloid cortex, the prepiriform area and the anterior amygdaloid
area, but do not reach the hippocampus.
ACKNOWLEDGEMENT
We wish to express our hearty thanks to Professor K. NnMI, Okayama University Medical School, and Professor T. ABURAYA, Tokushima University Medical School, for their kind
guidance and helpful suggestions throughout this investigation.
REFERENCES
1. ADEY, W. R. and MEYER, M.: Hippocampal and hypothalamic connexions of the
temporal lobe in the monkey. Brain 75, 358, 1952
2. ADEY, W. R., BUCHWALD, N. A. and LINDSLEY, D. F.: Amygdaloid, pallidal and
peripheral influences on mesencephalic unit firing patterns with reference to mechanisms
of tremor. EEG Clin. Neurophysiol. 12, 21, 1960
3. ADEY, W. R., RUDOLPH, A. F., HINE, I. F. and HARRIT, N. j.: Glees staining of the
monkey hypothalamus: a critical appraisal of normal and experimental material. j.
Anal. 92, 219, 1958
4. BAN, T. and OMUKAI, F.: Experimental studies on the fiber connections of the amygdaloid nuclei in the rabbit. j. Compo Neur. 113, 245, 1959
5. BERKELBACH van der SPRENKEL, H.: Stria terminalis and amygdala in the brain of the
opossum (Didelphis virginiana). ]. Compo Neur. 42, 211, 1926
6. COWAN, W. M., RAISMAN, G. and POWELL, T. P. S.: The connexions of the amygdala. j. Neur. Neurosurg. 28, 137, 1965
7. CROSBY, E. C. and HUMPHREY, T.: Studies of the vertebrate telencephalon. II. The
nuclear pattern of the anterior olfactory nucleus, tuberculum olfactorium and the amygdaloid complex in adult man. j. Compo Neur. 74, 309, 1941
8. Fox, C. A.: Certain bassal telencephalic centers in the cat. ]. Compo Neur. 72, 1. 1940
9. Fox, C. A.: The stria terminalis, longitudinal association bundle and precommissural
fornix fibers in the cat. j. Compo Neur. 79, 277, 1943
10. Fox, C. A.: Amygdalo-thalamic connections in Macaca mulatta. Anal. Rec. 103, 537,
1949
II. FUKUCHI, S.: Comparative-anatomical studies on the amygdaloid complex in mammals,
especially in ungulata. Fol. psychial. jap. 5. 241, 1952
12. GLOOR, P.: Electrophysiological studies on the connections of the amygdaloid nucleus
in the cat. I and II. EEG. Clin. N europhysiol. 7, 223, 1955
13. GLOOR, P.: Amygdala. Handbook of Physiology. ~ection I: Neurophysiology Vol. 2,
Williams & Wilkins, Baltimore, 1959
14. HALL, E. A.: Efferent connections of the basal and lateral nuclei of the amygdala in
the cat. Amer. j. Anal. 113, 139, 1963
15. JOHNSTON, j. B.: The evolution of the forebrain. j. Compo Neur. 35, 337, 1923
16. KARIBE, H.: Comparative anatomical studies on the amygdaloid complex, especially
in carnivora. Acla Insl. Anal. Niigala 50, 99, 1961 (in japanese)
17. KINGLER, j. and GLOOM, P.: The connections of the amygdala and of the anterior
http://escholarship.lib.okayama-u.ac.jp/amo/vol23/iss6/6
20
Ishikawa et al.: An experimental study on the efferent connections of the
Efferent Connections of Cat Amygdala
539
temporal cortex in the human brain. j. Camp. Neur. 115, 333, 1960
18. KOIKEGAMI, H.: Amygdala and other related limbic structures: Experimental studies
on the anatomy and function. 1. Anatomical researches with some neurophysiological
observations. Acta med. bioi. 10, 161, 1963
19. KOIKEGAMI, H., FUSE, S., YOKOYAMA, T., WATANABE, T. and WATANABE, H.: Contributions to the comparative anatomy of the amygdaloid nuclei of mammals with some
experiments of their destruction or stimulation. Foi. psychiat. jap. 8, 336, 1955
20. KUROTSU, T.: Studies on the autonomic center. Brain-Researches 3, 39, 1949 (in Japanese)
21. LAUER, E. W.: The nuclear pattern and fiber connections of certain basal telencephalic
centers in the macaque. j. Camp. Neur. 82, 215, 1945
22. NAUTA, W. J. H.: Fiber degeneration following lesions of the amygdaloid complex in
the monkey. j. Anat. 95, 515, 1961
23. NAUTA, W. J. H.: Neural association of the amygdaloid complex in the monkey. Brain
85, 505, 1962
24. NAUTA, W.J. H. and GYGAX, P. A.: Silver impregnation of degenerating axons in the
central nervous system: a modified technic. Stain T echn. 29, 91, 1954
25. POWELL, T. P. S., COWAN, W. M. and RAISMAN, G.: Olfactory relationships of the
diencephalon. Nature 199, 710, 1963
26. SNIDER, R. S. and NIEMER, W. T.: A Stereotaxic Atlas of the Cat frain. Univ. of
Chicago Press, Chicago, 1961
27. TAKAHASHI, K.: Experimental studies on the periamygdaloid cortex. Niigata Igakkai
Zasshi 66, 660, 1952 (in Japanese)
28. VALVERDE, F.: Amygdaloid Projection Field. Progress in Brain Research Vol. 3,20, 1963
29. VALVERDE, F.: Studies on the Piriform Lobe. Harvard Univ. Fress, Cambridge, 1965
30. YOUNG, M. W.: The nuclear pattern and fiber connections of the noncortical centers
of the telencephalan in the rabbit. j. Camp. Neur. 65, 295, 1963
Produced by The Berkeley Electronic Press, 1969
21